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All rights reserved First published online as a Review in Advance on January 12, 2004
Annu. Rev. Plant Biol. 2004.55:373-399. Downloaded from arjournals.annualreviews.org by CAPES on 12/19/08. For personal use only.
Institute of Plant Sciences, Swiss Federal Institute of Technology (ETH) Universit tstr. 2, 8092 Z rich, Switzerland a u 2 Max F. Perutz Laboratories, University of Vienna, Gregor-Mendel-Institute of Molecular Plant Sciences, Austrian Academy of Sciences, Vienna Biocenter, Dr. Bohrgasse 9, 1030 Vienna, Austria; email: heribert.hirt@unvie.ac.at
Key Words programmed cell death, abiotic stress, pathogen defense s Abstract Several reactive oxygen species (ROS) are continuously produced in plants as byproducts of aerobic metabolism. Depending on the nature of the ROS species, some are highly toxic and rapidly detoxied by various cellular enzymatic and nonenzymatic mechanisms. Whereas plants are surfeited with mechanisms to combat increased ROS levels during abiotic stress conditions, in other circumstances plants appear to purposefully generate ROS as signaling molecules to control various processes including pathogen defense, programmed cell death, and stomatal behavior. This review describes the mechanisms of ROS generation and removal in plants during development and under biotic and abiotic stress conditions. New insights into the complexity and roles that ROS play in plants have come from genetic analyses of ROS detoxifying and signaling mutants. Considering recent ROS-induced genomewide expression analyses, the possible functions and mechanisms for ROS sensing and signaling in plants are compared with those in animals and yeast.
CONTENTS
INTRODUCTION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . GENERATION OF ROS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Biotic Strategies to Generate ROS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Abiotic Strategies to Generate ROS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ROS DETOXIFICATION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Nonenzymatic ROS Scavenging Mechanisms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Enzymatic ROS Scavenging Mechanisms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . THE ROLE OF ROS IN SIGNALING . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ROS Sensing by Histidine Kinases . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ROS Activation of Mitogen-Activated Protein Kinase (MAPK) Signaling Pathways . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ROS Inhibition of Protein Phosphatases . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ROS Activation of Transcription Factors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1543-5008/04/0602-0373$14.00 374 374 375 377 380 380 381 382 383 383 384 384
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ROS AS SIGNALS FOR GENE EXPRESSION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ROS AT THE INTERFACE BETWEEN BIOTIC AND ABIOTIC STRESSES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ROS and Plant Pathogen Defense . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ROS and Abiotic Stress . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ROS and Stomata . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ROS and Roots . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . CONCLUSIONS AND OPEN QUESTIONS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Annu. Rev. Plant Biol. 2004.55:373-399. Downloaded from arjournals.annualreviews.org by CAPES on 12/19/08. For personal use only.
INTRODUCTION
The evolution of aerobic metabolic processes such as respiration and photosynthesis unavoidably led to the production of reactive oxyen species (ROS) in mitochondria, chloroplasts, and peroxisomes. A common feature among the different ROS types is their capacity to cause oxidative damage to proteins, DNA, and lipids. These cytotoxic properties of ROS explain the evolution of complex arrays of nonenzymatic and enzymatic detoxication mechanisms in plants. Increasing evidence indicates that ROS also function as signaling molecules in plants involved in regulating development and pathogen defense responses. In this review, we rst describe the biological effects and functions of ROS in plants and then discuss open questions that need to be addressed in future research.
GENERATION OF ROS
Ground state triplet molecular oxygen is a bioradical with its two outermost valence electrons occupying separate orbitals with parallel spins. To oxidize a nonradical atom or molecule, triplet oxygen would need to react with a partner that provides a pair of electrons with parallel spins that t into its free electron orbitals. However, pairs of electrons typically have opposite spins, and thus fortunately impose a restriction on the reaction of triplet molecular oxygen with most organic molecules (18, 51). However, ground state oxygen may be converted to the much more reactive ROS forms either by energy transfer or by electron transfer reactions. The former leads to the formation of singlet oxygen, whereas the latter results in the sequential reduction to superoxide, hydrogen peroxide, and hydroxyl radical (66) (Figure 1). In plants ROS are continuously produced as byproducts of various metabolic pathways localized in different cellular compartments (37). Under physiological steady state conditions these molecules are scavenged by different antioxidative defense components that are often conned to particular compartments (3). The equilibrium between production and scavenging of ROS may be perturbed by a number of adverse environmental factors. As a result of these disturbances, intracellular levels of ROS may rapidly rise (36, 74, 102, 120). Plants also generate ROS by activating various oxidases and peroxidases that produce ROS in response to certain environmental changes (1, 13, 14, 35, 109). The rapid increase in ROS
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Figure 1 Generation of different ROS by energy transfer or sequential univalent reduction of ground state triplet oxygen.
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concentration is called oxidative burst (5). External conditions that adversely affect the plants can be biotic, imposed by other organisms, or abiotic, arising from an excess or decit in the physical or chemical environment. Although plants responses to the various adverse environmental factors may show some commonalities, increases in ROS concentration triggered by either biotic or abiotic stresses are generally attributed to different mechanisms.
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cytosolic complex is recruited to the membrane, where it associates with the two membrane-bound components to assemble the active oxidase. Activation requires not only the assembly of the core components, but also the participation of two low molecular weight guanin-nucleotide-binding proteins (8). In addition to the NADPH-oxidase of phagocytes, other NADPH-oxidases also associated with plasma membranes are found in a variety of cells (8). Thus, the NADPH-oxidase activity originally described by Doke (35) may not necessarily represent a homologue of the leukocyte-specic enzyme. However, subsequent studies have provided several lines of evidence strongly suggesting a common origin for both enzymes. Antibodies raised against human p22PHOX, p47PHOX, and p67PHOX cross-reacted with plant proteins of similar sizes (32, 116), and in several plant species rboh genes (respiratory burst oxidase homologues) of p91PHOX, the catalytic subunit of the NADPH-oxidase of phagocytes, have been found (64, 119). In rice, homologues of GTP-binding proteins, required for activating the animal enzyme, have been implicated in pathogen-induced cell death (63), and the putative plant plasma membrane NADPH-oxidase reportedly produces superoxide (108). Finally, knock-out mutations of two Arabidopsis rboh genes, AtrbohD and AtrbohF, largely eliminate ROS production during disease resistance reactions of Arabidopsis to avirulent pathogens (118), thus providing direct genetic evidence that two components of a plant NADPH-oxidase are required for ROS production during plant defense responses. Homologues of the p47PHOX and p67PHOX regulators of the mammalian NADPH-oxidase were not found in the Arabidopsis genome (26), which suggests that the plant NADPH-oxidase may be regulated differently than that in mammalian macrophages. In addition to a plant-specic NADPH-oxidase, alternative mechanisms of ROS production have been proposed. Many peroxidases are localized in the apoplastic space and are ionically or covalently bound to cell wall polymers. Peroxidases can act in two different catalytic modes. In the presence of H2O2 and phenolic substrates they operate in the peroxidatic cycle and are engaged in the synthesis of lignin and other phenolic polymers. However, if the phenolic substrates are replaced by NADPH or related reduced compounds, a chain reaction starts that provides the basis for the H2O2-producing NADH-oxidase activity of peroxidases (22). Peroxidase H2O2 production is distinguished from that by the phagocyte-type NADPH-oxidase by different Km values for oxygen, different requirements for NADH and NADPH, and different sensitivities of the two enzymes to inhibitors such as cyanide, azide, and diphenyleneiodonium (DPI). Based on these differences rapid H2O2 production in some plant species triggered by pathogen attack and elicitor treatment has been attributed to the NAD(P)H-oxidase activity of apoplastic peroxidases (124). In addition to its NAD(P)H-oxidase activity that gives rise to superoxide and hydrogen peroxide, in vitro studies of horseradish peroxidase suggest another activity of this enzyme: generating hydroxyl radicals (22). Similar to the Fe2+/3+ catalyzed Haber-Weiss reaction, horseradish peroxidase can reduce hydrogen peroxide to hydroxyl radicals (22). Thus, one expects that whenever cell wallbound peroxidases
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come into contact with suitable concentrations of superoxide and H2O2, originating from the oxidative cycle of peroxidase or from other sources, hydroxyl radicals should form within the cell (110). This situation prevails, for instance, when O 2 and H2O2 levels are increased in plants in response to pathogen attack, followed by a hypersensitive reaction that leads to the death of host cells. However, producing hydroxyl radicals by cell wallbound peroxidases may also be relevant for other physiological responses such as the controlled breakdown of structural polymers during rearrangement of cell walls in roots, hypocotyls, or coleoptiles (40, 94, 126). In isolated tobacco epidermal cells two distinct ROS-producing mechanisms were activated after the addition of a fungal elicitor (1). One source of ROS production was identied as a NADPH-oxidase and/or a xanthine oxidase, whereas the second activity was attributed to a peroxidase and/or amine oxidase. It is not known whether these activities appear sequentially and thus are responsible for the two phases of ROS induction by fungal or bacterial elicitors that have been measured in plant cell cultures (9). Chewing herbivorous insects mechanically wound plant tissue while feeding and induce an increase in hydrogen peroxide levels inside the plant reminiscent of the oxygen burst triggered by pathogens (12, 16). Based on the inhibition by DPI H2O2 production was linked to the NADPH-oxidase (96), thus invoking a common mechanism for the production of H2O2 during plant-pathogen interaction and the wound response. Hydrogen peroxide has been proposed to act as a second messenger for the induction of defense genes in response to wounding. However, these defense genes are different from those induced during plant-pathogen interactions. Thus, the specicity of the wound-induced defense response may not be derived from H2O2. Because the selectivity of the inhibitor used in the study (96) has been questioned (1, 39), a different source of H2O2 production cannot be ruled out.
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Chlororespiration describes the reduction of oxygen resulting from the presence of a respiratory chain consisting of a NAD(P)H dehydrogenase and a terminal oxidase in chloroplasts that competes with the photosynthetic electron transport chain for reducing equivalents. This process has been largely studied in microalgae (11). Only recently have components of this respiratory chain also been found in higher plants (92). It is not known to what extent this process might contribute to ROS formation in chloroplasts of higher plants although the electron transport capacity of chlororespiration is only about <1% that of photosynthesis (e.g., 36a). The two primary processes involved in formation of ROS during photosynthesis are the direct photoreduction of O2 to the superoxide radical by reduced electron transport components associated with PSI and reactions linked to the photorespiratory cycle, including Rubisco in the chloroplast and glycolate-oxidase and CAT-peroxidase reactions in the peroxisome. When plants are exposed to light intensities that exceed the capacity of CO2 assimilation, overreduction of the electron transport chain leads to inactivation of PSII and the inhibition of photosynthesis. Plants may use two strategies to protect the photosynthetic apparatus against photoinhibition: rst, the thermal dissipation of excess excitation energy in the PSII antennae (nonphotochemical quenching), and second, the ability of PSII to transfer electrons to various acceptors within the chloroplast (photochemical quenching) (98). When plants are exposed to environmental stresses and the availability of CO2 within the leaf is restricted, as may occur, for example, under drought or temperature stress, the reduction of oxygen by PSI (Mehler reaction) (79) and the photorespiratory pathway play a critical photoprotective role (Figure 2). In leaves of C3 plants the photorespiratory oxygenation of ribulose 1,5bisphosphate by Rubisco constitutes a major alternative sink for electrons, thereby sustaining partial oxidation of PSII acceptors and preventing photoinactivation of PSII when CO2 availability is restricted. Rubisco catalyzes a competitive reaction in which oxygen is favored over CO2 as a substrate as temperature increases or as the intracellular CO2 concentration declines. This oxygenation reaction leads to the release of glycolate that is translocated from chloroplasts to peroxisomes. Its subsequent oxidation is catalyzed by the glycolate oxidase accounting for the major portion of H2O2 produced during photosynthesis (Figure 2). Oxygen reduction sustains signicant levels of photosynthetic electron ux not only through its role in photorespiration but also by its direct reduction by PSI (7) (Figure 2). Superoxide radicals generated by the one-electron reduction of molecular oxygen by PSI are rapidly converted within the chloroplast to hydrogen peroxide by CuZn-superoxide dismutase (7). It has been suggested that photoreduction of O2 to water by the Mehler ascorbate peroxidase pathway in intense light may involve up to 30% of the total electron transport (7). This would suggest that O2 plays an important role as an alternative electron acceptor in photoprotection. Producing large amounts of ROS is an inevitable consequence of the photosynthetic reduction of oxygen, and plants would have to evolve efcient strategies to cope with the accumulation of these potentially toxic compounds that are integral components of oxygenic photosynthesis.
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Figure 2 The principal features of photosynthetic electron transport under high light stress that lead to the production of ROS in chloroplasts and peroxisomes. Two electron sinks can be used to alleviate the negative consequences of overreduction of the photosynthetic electron chain: (a) the reduction of oxygen by PSI that generates superoxide and H2O2, and (b) the Rubisco oxygenase reaction and the photorespiratory pathway that lead to H2O2 generation within the peroxisome. Under light stress, increasing amounts of singlet oxygen are produced within PSII. Bold arrows show the main routes of electron transport. Key enzymes discussed in the text are shown in encircled numbers: 1) superoxide dismutase, 2) Rubisco, 3) glycolate oxidase, 4) catalase, and 5) ascorbate peroxidase.
Singlet Oxygen During photosynthesis singlet oxygen is continuously produced by PSII. The reaction center complex of PSII consists of cytochrome b559 and the heterodimer of the D1 and D2 proteins. The heterodimer binds the reaction centers functional prothestic groups including chlorophyll P680, pheophytin, and the quinone electron acceptors QA and QB. Excitation of the reaction center results in charge separation between P680 and pheophytin and the subsequent sequential reduction of QA and QB (10). When the redox state of the plastoquinone pool and QA and QB are overreduced because of excess light energy, charge separation cannot be completed and the oxidized P680 chlorophyll recombines with the reduced pheophytin. Under these conditions forming the triplet state of P680 is favored, leading to the generation of singlet oxygen by energy transfer. The release of singlet oxygen was rst detected in preparations of isolated PSII particles (73), but was subsequently shown to occur in vivo (41, 54). During excess light stress that leads to photoinhibition of PSII, singlet oxygen production drastically increases (53). In animals singlet oxygen may be produced metabolically during reduction of O2 catalyzed by the phagocytic NADPH-oxidase (113). A homologue of this enzyme is activated during plant-pathogen interaction. Thus, it is conceivable that singlet oxygen also takes part in defense reactions of plants. However, there is presently no data to support this proposal.
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MITOCHONDRIA In mammalian cells mitochondria are the major source of ROS (51). However, the relative contribution of mitochondria to ROS production in green tissues is very low (103). One reason that plant mitochondria do not produce more ROS could be the presence of the alternative oxidase (AOX) that catalyzes the tetravalent reduction of O2 by ubiquinone. The AOX competes with the cytochrome bc1 complex for electrons and thus may help to reduce ROS production in mitochondria. This suggestion is supported by ndings that H2O2 induces the expression of AOX (128), and overproduction of AOX in transgenic cell lines reduces ROS production, whereas antisense cells with reduced levels of the AOX accumulate ve times more ROS than control cells (77).
ROS DETOXIFICATION
In the presence of transition metal ions hydrogen peroxide may be reduced to hydroxyl radicals by superoxide. Superoxide and hydrogen peroxide are much less reactive than OH. The main risk for a cell that produces the two former reactive oxygen intermediates may be posed by the intermediates interaction, leading to the generation of highly reactive hydroxyl radicals. Because there are no known scavengers of hydroxyl radicals, the only way to avoid oxidative damage through this radical is to control the reactions that lead to its generation. Thus, cells had to evolve sophisticated strategies to keep the concentrations of superoxide, hydrogen peroxide, and transition metals such as Fe and Cu under tight control.
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Figure 3 The principal modes of enzymatic ROS scavenging by superoxide dismutase (SOD), catalase (CAT), the ascorbate-glutathione cycle, and the glutathione peroxidase (GPX) cycle. SOD converts hydrogen superoxide into hydrogen peroxide. CAT converts hydrogen peroxide into water. Hydrogen peroxide is also converted into water by the ascorbate-glutathione cycle. The reducing agent in the rst reaction catalyzed by ascorbate peroxidase (APX) is ascorbate, which oxidizes into monodehydroascorbate (MDA). MDA reductase (MDAR) reduces MDA into ascorbate with the help of NAD(P)H. Dehydroascorbate (DHA) is produced spontaneously by MDA and can be reduced to ascorbate by DHA reductase (DHAR) with the help of GSH that is oxidized to GSSG. The cycle closes with glutathione reductase (GR) converting GSSG back into GSH with the reducing agent NAD(P)H. The GPX cycle converts hydrogen peroxide into water using reducing equivalents from GSH. Oxidized GSSG is again converted into GSH by GR and the reducing agent NAD(P)H.
and results in enhanced tolerance towards oxidative stress induced in high light (27).
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H2O by APX occurs by oxidation of ascorbate to MDA (equation 1 in Figure 3c), which can be regenerated by MDA reductase (MDAR) using NAD(P)H as reducing equivalents (equation 2 in Figure 3c). MDA can spontaneously dismutate into dehydroascorbate. Ascorbate regeneration is mediated by dehydroascorbate reducatase (DHAR) driven by the oxidation of GSH to GSSG (Equation 3 in Figure 3c). Finally, glutathione reductase (GR) can regenerate GSH from GSSG using NAD(P)H as a reducing agent. Like APX, GPX also detoxies H2O2 to H2O, but uses GSH directly as a reducing agent (equation 1 in Figure 3d). The GPX cycle is closed by regeneration of GSH from GSSG by GR (equation 2 in Figure 3d). Unlike most organisms, plants have multiple genes encoding SOD and APX. Different isoforms are specically targeted to chloroplasts, mitochondria, peroxisomes, as well as to the cytosol and apoplast (6). Whereas GPX is cytoslic, CAT is located mainly in peroxisomes. Specic roles for antioxidant enzymes have been explored via transgenic approaches. Overexpression of tobacco chloroplast SOD to chloroplasts did not alter tolerance toward oxidative stress, which suggests that other antioxidant mechanisms might be limiting (2). However, expression of a pea chloroplast SOD in tobacco increased resistance to methyl viologeninduced membrane damage (2). CAT is indispensable for oxidative stress tolerance because transgenic tobacco plants with suppressed CAT have enhanced ROS levels in response to both abiotic and biotic stresses (130). The extent of oxidative stress in a cell is determined by the amounts of superoxide, H2O2, and hydroxyl radicals. Therefore, the balance of SOD, APX, and CAT activities will be crucial for suppressing toxic ROS levels in a cell. Changing the balance of scavenging enzymes will induce compensatory mechanisms. For example, when CAT activity was reduced in plants, scavenging enzymes such as APX and GPX were upregulated. Unexpected effects can also occur. When compared to plants with suppressed CAT, plants lacking both APX and CAT were less sensitive to oxidative stress (106). Because photosynthetic activity of these plants was decreased, reduction in APX and CAT might result in suppression of ROS production via chloroplasts.
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ROS other than H2O2 activate this as-1 element (42). Further analysis will reveal whether similarity exists among plant, animal, and fungal regulatory cis-elements of ROS-responsive genes.
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levels. An increase in expression of ROS detoxifying enzymes is compatible with compensatory mechanisms induced by oxidative stress. When tobacco plants decient in CAT were grown in high-intensity light, they increased ROS production and PR protein levels, and showed enhanced disease resistance (20).
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in some cases H2O2 is not required for PCD induction (46, 57). Studies show that a threshold exposure time of cells to H2O2 is required, during which period transcription and translation are necessary (34, 112). Pharmacological data indicate that removal of ROS during pathogen or elicitor challenge reduces PCD (34, 70). A recent genetic analysis conrms these data by showing that Arabidopsis knock-out lines lacking functional rboh genes (i.e., respiratory burst oxidase homolog genes) display reduced ROS generation and PCD following bacterial challenge (118). In line with this concept, tobacco plants with reduced CAT or ascorbate peroxidase expression show increased PCD to low doses of bacteria (83). It is not clear yet to what extent PCD in plants and animals share similar mechanisms. Expression of the animal cell death suppressor genes Bcl-xl and Ced-9 in tobacco plants suppresses oxidative stress-induced cell death (82). In animals, mitochondria play a primary role in ROS production and in triggering programmed cell death. Mitochondrial ROS production has also been implicated in eliciting ROS-induced cell death in plants (76, 117). However, as mentioned earlier, in plants the majority of ROS is produced in chloroplasts and peroxisomes. Whether or not these differences necessitated the evolution of different mechanisms of PCD in plants and animals is not known yet.
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apoplast. Future studies using plants with altered levels of ROS scavenging and/or ROS producing mechanisms might resolve this question.
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Depending on the character of the environmental stress, plants differentially enhance the release of ROS that are either chemically distinct or are generated within different cellular compartments (36, 91). For instance, during an incompatible plant-pathogen interaction, superoxide anions are produced enzymatically outside the cell and are rapidly converted to hydrogen peroxide that can cross the plasma membrane. The same ROS are also produced in chloroplasts exposed to high light stress, albeit by a different mechanism. The stress reactions of plants induced by pathogens differ from those induced by high light intensities (17, 52). If ROS act as signals that evoke these different stress responses, their biological activities should exhibit a high degree of selectivity and specicity that could be derived from their chemical identity and/or the intracellular locations where they were generated. Most of what is known about oxidant-induced signaling was found in experiments using hydrogen peroxide as an oxidant. In some of these experiments hydrogen peroxide was added to cell cultures or plants either directly (31) or indirectly by using H2O2-generating enzymes (4). In both cases the intracellular distribution of H2O2 is difcult to control and the physiological signicance of changes in gene expression that are induced under these conditions cannot easily be assessed. A more controlled release of H2O2 that is conned to specic compartments has become possible either by spraying plants with paraquat, a herbicide that under light generates H2O2 via superoxide predominantly within chloroplasts (79), or by modulating the expression of scavengers that are conned to different cellular compartments in transgenic plants (107, 121, 130). If one accepts the notion that the chemical identity of a given ROS and the cellular topography of its release contribute to the specicity of a stress response, it is hard to imagine how H2O2 alone could act as a signal that triggers such specic responses unless differences in the intracellular distribution of H2O2-responsive targets mediate such specicities of stress responses. As mentioned above it is also possible that hydroxyl radicals derived from hydrogen peroxide are the primary triggers of some stress responses in plants. In contrast to hydrogen peroxide, hydroxyl radicals are very unstable and restricted to subcompartmental regions. They may give rise to biologically active oxygenation products that could preserve some of the topographical information that may be necessary to ensure specicity of stress responses. Measuring global changes of gene expression in Arabidopsis cell cultures following treatment with hydrogen peroxide reveal major changes in gene expression (31). The surprisingly large number of genes that respond to an increase in hydrogen peroxide concentration would be in line with the proposed role of H2O2 as a ubiquitous signal for oxidative stress. However, the number of H2O2-responsive genes in cell culture was in marked contrast to that found in whole plants treated with low concentrations of paraquat (95). In the absence of visible necrotic lesions, very few genes were initially upregulated, some of which are intimately involved in the detoxication of H2O2, like ascorbate peroxidases I and II or ferritin I (62,
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100). These genes were different from those activated by singlet oxygen, which suggests that chemical differences between the two ROS might have contributed to the selectivity of the induced stress responses (95). This apparent selectivity was lost when plants were exposed to higher paraquat concentrations that led to visible lesion formation. Under these stress conditions the primary cause for a given stress response may be difcult to separate from secondary effects that are superimposed. This problem of discerning cause and effect has been highlighted in studies of tetrapyrrole biosynthesis and catabolism, in which several enzymatic steps were blocked experimentally (55, 72, 75, 84). A broad range of stress-related reactions were activated in these plants during illumination that have been attributed to the photodynamic activity of free tetrapyrrole intermediates that accumulated constitutively in these plants. However, many aspects of the responses are reminescent of those triggered by the release of superoxide and/or hydrogen peroxide during an incompatible plant-pathogen interaction (84). Either singlet oxygen, superoxide, and hydrogen peroxide may replace each other in triggering pathogen defense reactions, or the constitutive accumulation of photodynamically active tetrapyrrole intermediates and catabolites throughout the entire life cycle of these genetically modied plants may lead to photooxidative damage and injury that may promote a multifactorial induction of several overlapping secondary effects, some of which may mimic responses to pathogens. This latter interpretation agrees with in vivo measurements of ROS production in leaves under photooxidative stress, showing that singlet oxygen, superoxide, and hydrogen peroxide were produced simultaneously in the same leaf (41). If chemical specicity of a given ROS determines the specicity of stress responses, it would be difcult under these conditions to attribute a particular stress response to a well-dened ROS. So far very few case studies suggest a selective signaling effect of a given ROS (58, 69, 95). This may be due partially to the fact that most of the previous studies have focused on analyzing the signaling role of hydrogen peroxide andto a lesser extentsuperoxide radicals, whereas other ROS such as hydroxyl radicals and singlet oxygen have been largely ignored. As described earlier, there are several lines of evidence suggesting that hydroxyl radicals may not only be a noxious side product of oxygen metabolism but may play a more signicant role not only during oxidative stress but also during extension growth of roots, coleoptiles, and hypocotyls, or during seed germination. Singlet oxygen induces a specic set of stress responses (95). Its biological activity exhibits a high degree of selectivity that is derived from the chemical identity of this ROS and/or the intracellular location at which it is generated. These and other studies indicate that the biological activities of ROS may signicantly differ from each other. Hence, ndings from experiments with hydrogen peroxide as a model oxidant should not be inappropriately generalized and taken as a xed template for signaling events induced by all oxidants or by oxidative stress generated in a different way (66).
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ACKNOWLEDGMENTS This work was supported from grants from the Austrian and Swiss Science Foundations and the European Union.
The Annual Review of Plant Biology is online at http://plant.annualreviews.org
LITERATURE CITED
1. Allan AC, Fluhr R. 1997. Two distinct sources of elicited reactive oxygen species in tobacco epidermal cells. Plant Cell. 9:155972 2. Allen RD. 1995. Dissection of oxidative stress tolerance using transgenic plants. Plant Physiol. 107:104954 3. Alscher RG, Donahue JH, Cramer CL. 1997. Reactive oxygen species and antioxidants: relationships in green cells. Physiol. Plantarum. 100:22433 4. Alvarez ME, Pennell RI, Meijer P-J, Ishikawa A, Dixon RA, Lamb C. 1998. Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell 92:77384 5. Apostol I, Heinstein PF, Low PS. 1989. Rapid stimulation of an oxidative burst during elicidation of cultured plant cells. Role in defense and signal transduction. Plant Physiol. 90:10616 6. Asada K, Takahashi M. 1987. Production and scavenging of active oxygen in photosynthesis. In Photoinhibition, eds. DJ Kyle, CB Osborne, CJ Arntzen, pp. 227 87, Amsterdam: Elsevier 7. Asada K. 1999. The waterwater cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50:60139 8. Babior BM. 1999. NADPH oxidase: an update. Blood 93:146476 9. Baker MA, Orlandi EW. 1995. Active oxygen in plant pathogenesis. Annu. Rev. Phytopathol. 33:299321 10. Barber J. 1998. Photosystem two. Biochim. Biophys. Acta. 1365:26977 11. Bennoun P. 1982. Evidence for a respiratory chain in the chloroplast. Proc. Natl. Acad. Sci. USA 79:435256 Bi JL, Felton GW. 1995. Foliar oxidative stress and insect herbivory: primary compounds, secondary metabolites and reactive oxygen species as components of induced resistance. J. Chem. Ecol. 151130 Bolwell GP, Bindschedler LV, Blee KA, Butt VS, Davies DR, et al. 2002. The apoplastic oxidative burst in response to biotic stress in plants: a three-component system. J. Exp. Bot. 53:136776 Bolwell GP, Davies DR, Gerrish C, Auh CK, Murphy TM. 1998. Comparative biochemistry of the oxidative burst produced by rose and french bean cells reveals two distinct mechanisms. Plant Physiol. 116:137985 Bolwell GP. 1999. Role of active oxygen species and NO in plant defense responses. Curr. Opin. Plant Biol. 2:28794 Bradley DJ, Kjellbom P, Lamb CJ. 1992. Elicitor- and wound-induced oxidative cross-linking of a proline-rich plant cellwall protein: A novel, rapid defense response. Cell 70:2130 Bray EA, Bailey-Serres J, Weretilnyk E. 2000. Responses to abiotic stresses. In Biochemistry and Molecular Biology of Plants, eds. BB Buchanan, W Gruissem and RL Jones, pp. 1158203. Rockville, MD: Am. Soc. Plant Physiol. Cadenas E. 1989. Biochemistry of oxygen toxicity. Annu. Rev. Biochem. 58:79110 Causton HC, Ren B, Koh SS, Harbison CT, Kanin E, et al. 2001. Remodeling of yeast genome expression in response to environmental changes. Mol. Biol. Cell 12:32337
Annu. Rev. Plant Biol. 2004.55:373-399. Downloaded from arjournals.annualreviews.org by CAPES on 12/19/08. For personal use only.
12.
13.
14.
15.
16.
17.
18. 19.
ROS 20. Chamnongpol S, Willekens H, Moeder W, Langebartels C, Sandermann H Jr, et al. 1998. Defense activation and enhanced pathogen tolerance induced by H2O2 in transgenic tobacco. Proc. Natl. Acad. Sci. USA 95:581823 21. Chen D, Toone WM, Mata J, Lyne R, Burns G, et al. 2003. Global transcriptional responses of ssion yeast to environmental stress. Mol. Biol. Cell 14:214 29 22. Chen SX, Schopfer P. 1999. Hydroxylradical production in physiological reactions. A novel function of peroxidase. Eur. J. Biochem. 260:72635 23. Conklin PL, Williams EH, Last RL. 1996. Environmental stress sensitivity of an ascorbic acid-decient Arabidopsis mutant. Proc. Natl. Acad. Sci. USA 93:9970 74 24. Creissen G, Firmin J, Fryer M, Kular B, Leyland N, et al. 1999. Elevated glutathione biosynthetic capacity in the chloroplasts of transgenic tobacco plants paradoxically causes increased oxidative stress. Plant Cell 11:127792 25. Dalton TP, Shertzer HG, Puga A. 1999. Regulation of gene expression by reactive oxygen. Annu. Rev. Pharmacol. Toxicol. 39:67101 26. Dangl JL, Jones JDG. 2001. Plant pathogens and integrated defense responses to infection. Nature 411:82633 27. Davison PA, Hunter CN, Horton P. 2002. Overexpression of -carotene hydroxylase enhances stress tolerance in Arabidopsis. Nature 418:2036 28. Delaunay A, Isnard A-D, Toledano MB. 2000. H2O2 sensing through oxidation of the Yap1 transcription factor. EMBO J. 19:515766 29. Delaunay A, Pieger D, Barrault MB, Vinh J, Toledano MB. 2002. A thiol peroxidase is an H2O2 receptor and redox-transducer in gene activation. Cell 111:47181 30. Delledonne M, Zeier J, Marocco A, Lamb C. 2001. Signal interactions between ni-
393
31.
32.
33.
34.
35.
36.
36a.
37.
38.
tric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response. Proc. Natl. Acad. Sci. USA 98:1345459 Desikan R, A-H Mackerness S, Hancock JT, Neill SJ. 2001. Regulation of the Arabidopsis transcriptome by oxidative stress. Plant Physiol. 127:15972 Desikan R, Hancock JT, Coffey MJ, Neill SJ. 1996. Generation of active oxygen in elicited cells of Arabidopsis thaliana is mediated by a NADPH oxidase-like enzyme. FEBS Lett. 382:21317 Desikan R, Neill SJ, Hancock JT. 2000. Hydrogen peroxide-induced gene expression in Arabidopsis thaliana. Free Rad. Biol. Med. 28:77378 Desikan R, Reynolds A, Hancock JT, Neill SJ. 1998. Harpin and hydrogen peroxide both initiate programmed cell death but have differential effects on gene expression in Arabidopsis suspension cultures. Biochem. J. 330:11520 Doke N. 1985. NADPH-dependent O2generation in membrane fractions isolated from wounded potato tubers inoculated with Phytophtora infestans. Physiol. Plant Pathol. 27:31122 Elstner EF. 1991. Mechanisms of oxygen activation in different compartments of plant cells. In Active Oxygen/Oxidative Stress in Plant Metabolis, eds. EJ Pelland, KL Steffen. pp.1325. Rockville, MD: Am. Soc. Plant Physiol. Feild TS, Nedbal L, Ort DR. 1998. Nonphotochemical reduction of the plastoquinone pool in sunower leaves originates from chlororespiration. Plant Physiol. 116:120918 Foyer CH, Harbinson JC. 1994. Oxygen metabolism and the regulation of photosynthetic electron transport. In Causes of Photooxidative Stress and Amelioration of Defense Systems in Plant, eds. CH Foyer, PM Mullineaux. pp. 142. Boca Raton, Fla.: CRC Foyer CH, Noctor G. 2000. Oxygen processing in photosynthesis: regulation
Annu. Rev. Plant Biol. 2004.55:373-399. Downloaded from arjournals.annualreviews.org by CAPES on 12/19/08. For personal use only.
394
APEL
HIRT trol of protein tyrosine phosphatases and mitogen-activated protein kinases in plants. Plant Physiol. 132:114952 Gustin MC, Albertyn J, Alexander M, Davenport K. 1998. MAP kinase pathways in the yeast Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 62:1264300 Halliwell B, Gutteridge JMC. 1989. Free Radicals in Biology and Medicine, 2nd ed., Oxford: Clarendon Hammond-Kosack K, Jones JDG. 2000. Responses to plant pathogens. In Biochemistry and Molecular Biology of Plants, eds. BB Buchanan, W Gruissem, RL Jones. pp. 1102156. Rockville, MD: Am. Soc. Plant Physiol. Hideg E, Barta C, Kalai T, Vass I, Hideg K, Asada K. 2002. Detection of singlet oxygen and superoxide with uorescent sensors in leaves under stress by photo inhibition or UV radiation. Plant Cell Physiol. 43:115464 Hideg E, Kalai T, Hideg K, Vass I. 1998. Photoinhibition of photosynthesis in vivo results in singlet oxygen production. Detection via nitroxide-induced uorescence quenching in broad bean leaves. Biochemistry 37:1140511 Hu G, Yalpani N, Briggs SP, Johal GS. 1998. A porphyrin pathway impairment is responsible for the phenotype of a dominant disease lesion mimic mutant of maize. Plant Cell 10:1095105 Hwang I, Chen H-C, Sheen J. 2002. Twocomponent signal transduction pathways in Arabidopsis. Plant Physiol. 129:500 15 Ichinose Y, Andi S, Doi R, Tanaka R, Taguchi F, et al. 2001. Generation of hydrogen peroxide is not required for harpin-induced apoptotic cell death in tobacco BY-2 cell suspension cultures. Plant Physiol. Biochem. 39:77176 Jabs T, Dietrich RA, Dangl JL. 1996. Initiation of runaway cell death in an Arabidopsis mutant by extracellular superoxide. Science 273:185356
39.
40.
41.
42.
43.
44. 45.
46.
47.
48.
49.
and signaling. New Phytol. 146:359 88 Frahry G, Schopfer P. 1998. Inhibition of O2-reducing activity of horseradish peroxidase by diphenyleneiodonium. Phytochemistry 48:22327 Frahry G, Schopfer P. 2001. NADHstimulated, cyanide-resistant superoxide production in maize coleoptiles analyzed with a tetrazolium-based assay. Planta 212:17583 Fryer MJ, Oxborough K, Mullineaux PM, Baker NR. 2002. Imaging of photooxidative stress responses in leaves. J. Exp. Bot. 53:124954 Garreton V, Carpinelli J, Jordana X, Holuigue L. 2002. The as-1 promoter element is an oxidative stress-responsive element and salicylic acid activates it via oxidative species. Plant Physiol. 130:1516 26 Gasch A, Spellman P, Kao C, Harel O, Eisen M, et al. 2000. Genomic expression programs in the response of yeast cells to environmental changes. Mol. Biol. Cell 11:424157 Georgiou G. 2002. How to ip the (redox) switch. Cell 111:60710 Girotti AW. 2001. Photosensitized oxidation of membrane lipids: reaction pathways, cytotoxic effects and cytoprotective mechanisms. J. Photochem. Photobiol. 63:10313 Glazener JA, Orlandi EW, Baker CJ. 1996. The active oxygen response of cell suspensions to incompatible bacteria is not sufcient to cause hypersensitive cell death. Plant Physiol. 110:75963 Grant JJ, Loake GJ. 2000. Role of reactive oxygen intermediates and cognate redox signaling in disease resistance. Plant Physiol. 124:2129 Grether-Beck S, Bonizzi G, SchmittBrenden H, Felsner I, Timmer A, et al. 2000. Non-enzymatic triggering of the ceramide signaling cascade by solar UVA radiation. EMBO J. 19:5793800 Gupta R, Luan S. 2003. Redox con-
50.
51.
Annu. Rev. Plant Biol. 2004.55:373-399. Downloaded from arjournals.annualreviews.org by CAPES on 12/19/08. For personal use only.
52.
53.
54.
55.
56.
57.
58.
ROS 59. Jonak C, Okresz L, B gre L, Hirt H. 2002. o Complexity, cross talk and integration of plant MAP kinase signaling. Curr. Opin. Plant Biol. 5:41524 60. Joo JH, Bae YS, Lee JS. 2001. Role of auxin-induced reactive oxygen species in root gravitropism. Plant Physiol. 126:105560 61. Karin M, Liu Z, Zandi E. 1997. AP-1 function and regulation. Curr. Opin. Cell Biol. 9:24046 62. Karpinski S, Reynolds H, Karpinska B, Wingsle G, Creissen J, Mullineaux PC. 1999. Systemic signaling and acclimation in response to excess excitation energy in Arabidopsis. Science 284:65457 63. Kawasaki T, Henmi K, Ono E, Hatakeyama S, Iwano M, et al. 1999. The small GTP-binding protein Rac is a regulator of cell death in plants. Proc. Natl. Acad. Sci. USA 96:1092226 64. Keller T, Danude HG, Werner D, Doerner P, Dixon RA, Lamb C. 1998. A plant homolog of the neutrophil NADPH oxidase gp91phox subunit gene encodes a plasma membrane protein with Ca2+ binding motifs. Plant Cell. 10:25566 65. Klessig DF, Durner J, Noad R, Navarre DA, Wendehenne D, et al. 2000. Nitric oxide and salicylic acid signaling in plant defense. Proc. Natl. Acad. Sci. USA 97:884955 66. Klotz L-O. 2002. Oxidant-induced signaling: effects of peroxynitrite and singlet oxygen. Biol. Chem. 383:44356 67. Kovtun Y, Chiu W-L, Tena G, Sheen J. 2000. Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. Proc. Natl. Acad. Sci. USA 97:294045 68. Lee S, Choi H, Suh S, Doo I-S, Oh K-Y, et al. 1999. Oligogalacturonic acid and chitosan reduce stomatal aperture by inducing the evolution of reactive oxygen species from guard cells of tomato and Commelina communis. Plant Physiol. 121:14752 69. Leisinger U, Rufenacht K, Fischer B, Pe-
395
70.
71.
72.
73.
74.
75.
76.
77.
78.
saro M, Spengler A, et al. 2001. The glutathione peroxidase homologous gene from Chlamydomonas reinhardtii is transcriptionally up-regulated by singlet oxygen. Plant Mol. Biol. 46:395408 Levine A, Tenhaken R, Dixon R, Lamb C. 1994. H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79:58393 Low PS, Merida JR. 1996. The oxidative burst in plant defense: function and signal transduction. Physiol. Plant. 96:53342 Mach JM, Castillo AR, Hoogstraten R, Greenberg JT. 2001. The Arabidopsisaccelerated cell death gene ACD2 encodes red chlorophyll catabolite reductase and suppresses the spread of disease symptoms. Proc. Natl. Acad. Sci. USA 98:77176 Macpherson AN, Telfer A, Barber J, Truscott TG. 1993. Direct detection of singlet oxygen from isolated photosystem II reaction centres. Biochim. Biophys. Acta 1143:3019 Malan C, Gregling MM, Gressel J. 1990. Correlation between CuZn superoxide dismutase and glutathione reductase and environmental and xenobiotic stress tolerance in maize inbreds. Plant Sci. 69:157 66 Matringe M, Camadro JM, Labbe P, Scalla R. 1989. Protoporphyrinogen oxidase as a molecular target for diphenylether herbicides. Biochem. J. 260:23135 Maxwell DP, Nickels R, McIntosh L. 2002. Evidence of mitochondrial involvement in the transduction of signals required for the induction of genes associated with pathogen attack and senescence. Plant J. 29:26979 Maxwell DP, Wang Y, McIntosh L. 1999. The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. Proc. Natl. Acad. Sci. USA 96:8271 76 McAinsh MR, Clayton H, Manseld TA, Hetherington AM. 1996. Changes in stomatal behaviour and guard cell
Annu. Rev. Plant Biol. 2004.55:373-399. Downloaded from arjournals.annualreviews.org by CAPES on 12/19/08. For personal use only.
396
APEL
HIRT 87. Mou Z, Fan W, Dong X. 2003. Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113:93544 88. Mullineaux P, Karpinski S. 2002. Signal transduction in response to excess light: getting out of the chloroplast. Curr. Opin. Plant Biol. 5:4348 89. Murata Y, Pei Z-M, Mori IC, Schroeder J. 2001. Abscisic acid activation of plasma membrane Ca2+ channels in guard cells requires cytosolic NAD(P)H and is differentially disrupted upstream and downstream of reactive oxygen species production in abi1-1 and abi2-1 protein phosphatase 2C mutants. Plant Cell. 13:251323 90. Mustilli A-C, Merlot S, Vavasseur A, Fenzi F, Giraudat J. 2002. Arabidopsis OST1 protein kinase mediates the regulation of stomatal aperture by abscisic acid and acts upstream of reactive oxygen species production. Plant Cell 14:3089 99 91. Neill N, Desikan R, Hancock J. 2002. Hydrogen peroxide signaling. Curr. Opin. Plant Biol. 5:38895 92. Nixon PJ. 2000. Chlororespiration. Philos. Trans. R. Soc. London B 355:154147 93. Noctor G, Gomez L, Vanacker H, Foyer CH. 2002. Interactions between biosynthesis, compartmentation and transport in the control of glutathione homeostasis and signaling. J. Exp. Bot. 53:1283304 94. Ogawa K, Kanematsu S, Asada K. 1997. Generation of superoxide anion and localization of CuZn-superoxide dismutase in the vascular tissue of spinach hypocotyls: their association with lignication. Plant Cell Physiol. 38:111826 95. op den Camp RG, Przybyla D, Ochsenbein C, Laloi C, Kim C, et al. 2003. Rapid induction of distinct stress responses following the release of singlet oxygen in Arabidopsis thaliana. Plant Cell 15:2320 32 96. Orozco-Cardenas ML, Narvaez-Vasquez J, Ryan CA. 2001. Hydrogen peroxide
79.
80.
81.
82.
83.
84.
85.
86.
cytosolic free calcium in response to oxidative stress. Plant Physiol. 111:103142 Mehler AH. 1951. Studies on reactions of illuminated chloroplasts. II Stimulation and inhibition of the reaction with molecular oxygen. Arch. Biochem. Biophys. 33:33951 Meinhard M, Grill E. 2001. Hydrogen peroxide is a regulator of ABI1, a protein phosphatase 2C from Arabidopsis. FEBS Lett. 508:44346 Meinhard M, Rodriguez PL, Grill E. 2002. The sensitivity of ABI2 to hydrogen peroxide links the abscisic acid-response regulator to redox signaling. Planta 214:775 82 Mitsuhara I, Malik KA, Miura M, Ohashi Y. 1999. Animal cell-death suppressors Bcl-xL and Ced-9 inhibit cell death in tobacco plants. Curr. Biol. 9:77578 Mittler R, Herr EH, Orvar BL, van Camp W, Willekens H, et al. 1999. Transgenic tobacco plants with reduced capability to detoxify reactive oxygen intermediates are hyperresponsive to pathogen infection. Proc. Natl. Acad. Sci. USA 96:1416514170 Mock HP, Heller W, Molina A, Neubohn B, Sandermnann H, Grimm B. 1999. Expression of uroporphyrinogen decarboxylase or coproporphyrinogen oxidase antisense RNA in tobacco induces pathogen defense responses conferring increased resistance to tobacco mosaic virus. J. Biol. Chem. 274:423138 Moon H, Lee B, Choi G, Shin D, Prasad T, et al. 2003. NDP kinase 2 interacts with two oxidative stress-activated MAPKs to regulate cellular redox state and enhances multiple stress tolerance in transgenic plants. Proc. Natl. Acad. Sci. USA 100:35863 Moseyko N, Zhu T, Chang HS, Wang X, Feldman LJ. 2002. Transcription proling of the early gravitropic response in Arabidopsis using high-density oligonucleotide probe microarrays. Plant Physiol. 130:72028
Annu. Rev. Plant Biol. 2004.55:373-399. Downloaded from arjournals.annualreviews.org by CAPES on 12/19/08. For personal use only.
ROS acts as a second messenger for the induction of defense genes in tomato plants in response to wounding, systemin, and methyl jasmonate. Plant Cell. 13:17991 Orozco-Cardenas ML, Ryan C. 1999. Hydrogen peroxide is generated systemically in plant leaves by wounding and systemin via the octadecanoid pathway. Proc. Natl. Acad. Sci. USA 96:655357 Ort RD, Baker NR. 2002. A photoprotective role for O2 as an alternative electronic sink in photosynthesis? Curr. Opin. Plant Biol. 5:19398 Pei Z-M, Murata Y, Benning G, Thomine S, Klusener B, et al. 2000. Calcium channels activated by hydrogen peroxide mediate abscisic signaling in guard cells. Nature 406:73134 Petit J-M, Briat J-F, Lobr aux S. 2001. e Structure and differential expression of the four members of the Arabidopsis thaliana ferritin gene family. Biochem. J. 359:57582 Polidoros AN, Mylona PV, Scandalios JG. 2001. Transgenic tobacco plants expressing the maize Cat2 gene have altered catalase levels that affect plant-pathogen interactions and resistance to oxidative stress. Transgenic Res. 10:55569 Prasad TK, Anderson MD, Martin BA, Stewart CR. 1994. Evidence for chilling-induced oxidative stress in maize seedlings and a regulatory role for hydrogen peroxide. Plant Cell. 6:6574 Purvis AC. 1997. Role of the alternative oxidase in limiting superoxide production by plant mitochondria. Physiol. Plant. 100:16570 Quinn J, Findlay VJ, Dawson K, Millar JB, Jones N, et al. 2002. Distinct regulatory proteins control the graded transcriptional response to increasing H(2)O(2) levels in ssion yeast Schizosaccharomyces pombe. Mol. Biol. Cell. 13:805 16 Rebeiz CA, Montazer-Zouhoor A, Mayasich JM, Tripathy BC, Wu S-M, Rebeiz C. 1988. Photodynamic herbicides. Recent
397
106.
97.
98.
Annu. Rev. Plant Biol. 2004.55:373-399. Downloaded from arjournals.annualreviews.org by CAPES on 12/19/08. For personal use only.
107.
99.
108.
100.
101.
109.
102.
110.
103.
111.
104.
112.
105.
113.
developments and molecular basis of selectivity. CRC Crit. Rev. Plant Sci. 6:385 436 Rizhsky L, Hallak-Herr E, Van Breusegem F, Rachmilevitch S, Barr JE, et al. 2002. Double antisense plants lacking ascorbate peroxidase and catalase are less sensitive to oxidative stress than single antisense plants lacking ascorbate peroxidase or catalase. Plant J. 32:32942 Roxas VP, Smith RK, Allen ER, Allen RD. 1997. Overexpression of glutathione S-transferase/glutathione peroxidase enhances the growth of transgenic tobacco seedlings during stress. Nat. Biotechnol. 15:98891 Sagi M, Fluhr R. 2001. Superoxide production by plant homologues of the gp91phox NADPH oxidase. Modulation of activity by calcium and by tobacco mosaic virus infection. Plant Physiol. 126:128190 Schopfer P, Plachy C, Frahry G. 2001. Release of reactive oxygen intermediates (superoxide radicals, hydrogen peroxide, and hydroxyl radicals) and peroxidase in germinating radish seeds controlled by light, gibberellin and abscisic acid. Plant Physiol. 125:1591602 Schopfer P. 2001. Hydroxyl radicalinduced cell-wall loosening in vitro and in vivo: implications for the control of elongation growth. Plant J. 28:67988 Singh KK. 2000. The Saccharomyces cerevisiae SLN1P-SSK1P two component system mediates response to oxidative stress and in an oxidant-specic fashion. Free Rad. Biol. Med. 29:104350 Solomon M, Belenghi B, Delledonne M, Menachem E, Levine A. 1999. The involvement of cysteine proteases and protease inhibitor genes in the regulation of programmed cell death in plants. Plant Cell 11:43143 Steinbeck MJ, Khan AU, Karnovsky MJ. 1992. Intracellular singlet oxygen generation by phagocytosing neutrophils
398
APEL
HIRT Carr R, Jhoti H. 2003. Oxidation state of the active-site cysteine in protein tyrosine phosphatase 1B. Nature 423:77377 Vanacker H, Carver TLW, Foyer CH. 2000. Early H2O2 accumulation in mesophyll cells leads to induction of glutathione during the hypersensitive response in the barley-powdery mildew interaction. Plant Physiol. 123:1289300 Vera-Estrella R, Blumwald E, Higgins VJ. 1992. Effect of specic elicitors of Cladosporium fulvum on tomato suspension cells. Evidence for the involvement of active oxygen species. Plant Physiol. 99:120815 Vernoux T, Sanchez-Fernandez R, May M. 2002. Glutathione biosynthesis in plants. In Oxidative Stress in Plants, eds. D Inze, MV Montagu. pp. 297311. London: Taylor and Francis Vianello A, Macri F. 1991. Generation of superoxide anion and hydrogen peroxide at the surface of plant cells. J. Bioenerg. Biomembr. 23:40923 Vranova E, Atichartpongkul S, Villarroel R, Van Montagu M, Inze D, Van Camp W. 2002. Comprehensive analysis of gene expression in Nicotiana tabacum leaves acclimated to oxidative stress. Proc. Natl. Acad. Sci. USA 99:1087075 Wagner AM. 1995. A role for active oxygen species as second messengers in the induction of alternative oxidase gene expression in Petunia hybrida cells. FEBS Lett. 368:33942 Whistler CA, Corbell NA, Sarniguet A, Ream W, Loper JE. 1998. The twocomponent regulators GacS and GacA inuence accumulation of the stationaryphase sigma factor sigmaS and the stress response in Pseudomonas uorescens Pf5. J. Bacteriol. 180:663541 Willekens H, Chamnongpol S, Davey M, Schraudner M, Langebartels C, et al. 1997. Catalase is a sink for H2O2 and is indispensable for stress defense in C3 plants. EMBO J. 16:480616 Wohlgemuth H, Mittelstrass K,
114.
115.
116.
117.
118.
119.
120.
121.
122.
in response to particles coated with a chemical trap. J. Biol. Chem. 267:1342533 Sweetlove LJ, Heazlewood JL, Herald V, Holtzapffel R, Day DA, et al. 2002. The impact of oxidative stress on Arabidopsis mitochondria. Plant J. 32:891904 Takeda T, Toda T, Kominami K, Kohnosu A, Yanagida M, Jones N. 1995. Schizosaccharomyces pombe atf1+ encodes a transcription factor required for sexual development and entry into stationary phase. EMBO J. 14:6193208 Tenhaken R, Levine A, Brisson LF, Dixon RA, Lamb C. 1995. Function of the oxidative burst in hypersensitive disease resistance. Proc. Natl. Acad. Sci. USA 92:415863 Tiwari BS, Belenghi B, Levine A. 2002. Oxidative stress increased respiration and generation of reactive oxygen species, resulting in ATP depletion, opening of mitochondrial permeability transition, and programmed cell death. Plant Physiol. 128:127181 Torres MA, Dangl JL, Jones JDG. 2002. Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc. Natl. Acad. Sci. USA 99:51722 Torres MA, Onouchi H, Hamada S, Machida C, Hammond-Kossack KE, Jones JDG. 1998. Six Arabidopsis thaliana homologues of the human respiratory burst oxidase (gp91phox). Plant J. 14:36570 Tsugane K, Kobayashi K, Niwa Y, Ohba Y, Wada K, Kobayashi H. 1999. A recessive Arabidopsis mutant that grows enhanced active oxygen detoxication. Plant Cell. 11:1195206 van Breusegem F, Slooten L, Stassart JM, Moens T, Botterman J, et al. 1999. Overproduction of Arabidopsis thaliana FeSOD confers oxidative stress tolerance to transgenic maize. Plant Cell Physiol. 40:51523 van Montfort RL, Congreve M, Tisi D,
123.
124.
Annu. Rev. Plant Biol. 2004.55:373-399. Downloaded from arjournals.annualreviews.org by CAPES on 12/19/08. For personal use only.
125.
126.
127.
128.
129.
130.
131.
ROS Kschieschan S, Bender J, Weigel H-J, et al. 2002. Activation of an oxidative burst is a general feature of sensitive plants exposed to the air pollutant ozone. Plant Cell Environ. 25:71726 132. Zhang X, Zhang L, Dong F, Gao J, Galbraith DW, Song C-P. 2001. Hydrogen
399
peroxide is involved in abscisic acidinduced stomatal closure in Vicia faba. Plant Physiol. 126:143848 133. Zheng M, Aslund F, Storz G. 1998. Activation of the OxyR transcription factor by reversible disulde bond formation. Science 279:171821
Annu. Rev. Plant Biol. 2004.55:373-399. Downloaded from arjournals.annualreviews.org by CAPES on 12/19/08. For personal use only.
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Figure 4 Schematic depiction of cellular ROS sensing and signaling mechanisms. ROS sensors such as membrane-localized histidine kinases can sense extracellular and intracellular ROS. Intracellular ROS can also influence the ROS-induced mitogen-activated protein kinase (MAPK) signaling pathway through inhibition of MAPK phosphatases (PPases) or downstream transcription factors. Whereas MAP kinases regulate gene expression by altering transcription factor activity through phosphorylation of serine and threonine residues, ROS regulation occurs by oxidation of cysteine residues.
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Figure 5 Different roles of ROS under conditions of (a) pathogen attack or (b) abiotic stress. Upon pathogen attack, receptor-induced signaling activates plasma membrane or apoplast-localized oxidases that produce superoxide radicals (O) that are 2 highly toxic and can help to kill the invading pathogen. On the other hand, O2 is rapidly dismutated into hydrogen peroxide, which, in contrast to superoxide, can readily cross the plasma membrane. Intracellular ROS levels increase due not only to extracellular production of ROS but also by downregulation of ROS scavenging mechanisms. Overall, ROS amounts increase to critical levels and induce programmed cell death (PCD). During abiotic stress, ROS production occurs mainly in chloroplasts and mitochondria at the sites of electron transport, increasing intracellular ROS amounts to toxic levels. The cellular response encompasses upregulation of ROS scavenging mechanisms to detoxify increased amounts of ROS.
CONTENTS
Annu. Rev. Plant Biol. 2004.55:373-399. Downloaded from arjournals.annualreviews.org by CAPES on 12/19/08. For personal use only.
DNA METHYLATION AND EPIGENETICS, Judith Bender PHOSPHOENOLPYRUVATE CARBOXYLASE: A NEW ERA OF STRUCTURAL BIOLOGY, Katsura Izui, Hiroyoshi Matsumura,
Tsuyoshi Furumoto, and Yasushi Kai
69 85
METABOLIC CHANNELING IN PLANTS, Brenda S.J. Winkel RHAMNOGALACTURONAN II: STRUCTURE AND FUNCTION OF A BORATE CROSS-LINKED CELL WALL PECTIC POLYSACCHARIDE,
Malcolm A. ONeill, Tadashi Ishii, Peter Albersheim, and Alan G. Darvill
109
NATURALLY OCCURRING GENETIC VARIATION IN ARABIDOPSIS THALIANA, Maarten Koornneef, Carlos Alonso-Blanco, and
Dick Vreugdenhil 141
SINGLE-CELL C4 PHOTOSYNTHESIS VERSUS THE DUAL-CELL (KRANZ) PARADIGM, Gerald E. Edwards, Vincent R. Franceschi,
and Elena V. Voznesenskaya 173 197 225 263 289 315
PHYTOESTROGENS, Richard A. Dixon DECODING Ca2+ SIGNALS THROUGH PLANT PROTEIN KINASES,
Jeffrey F. Harper, Ghislain Breton, and Alice Harmon
PLASTID TRANSFORMATION IN HIGHER PLANTS, Pal Maliga SYMBIOSES OF GRASSES WITH SEEDBORNE FUNGAL ENDOPHYTES,
Christopher L. Schardl, Adrian Leuchtmann, Martin J. Spiering
TRANSPORT MECHANISMS FOR ORGANIC FORMS OF CARBON AND NITROGEN BETWEEN SOURCE AND SINK, Sylvie Lalonde,
Daniel Wipf, and Wolf B. Frommer 341
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viii
CONTENTS
REACTIVE OXYGEN SPECIES: METABOLISM, OXIDATIVE STRESS, AND SIGNAL TRANSDUCTION, Klaus Apel and Heribert Hirt THE GENERATION OF Ca2+ SIGNALS IN PLANTS,
Alistair M. Hetherington and Colin Brownlee
BIOSYNTHESIS AND ACCUMULATION OF STEROLS, Pierre Benveniste HOW DO CROP PLANTS TOLERATE ACID SOILS? MECHANISMS OF ALUMINUM TOLERANCE AND PHOSPHOROUS EFFICIENCY,
Leon V. Kochian, Owen A. Hoekenga, and Miguel A. Pi eros n
Annu. Rev. Plant Biol. 2004.55:373-399. Downloaded from arjournals.annualreviews.org by CAPES on 12/19/08. For personal use only.
VIGS VECTORS FOR GENE SLIENCING: MANY TARGETS, MANY TOOLS, Dominique Robertson GENETIC REGULATION OF TIME TO FLOWER IN ARABIDOPSIS THALIANA,
Yoshibumi Komeda
INDEXES
Subject Index Cumulative Index of Contributing Authors, Volumes 4555 Cumulative Index of Chapter Titles, Volumes 4555 629 661 666
ERRATA
An online log of corrections to Annual Review of Plant Biology chapters may be found at http://plant.annualreviews.org/